Ecotoxicology of Amphibians and Reptiles Second Edition 64169.indb 1 5/3/10 10:19:45 AM Other Titles from the Society of Environmental Toxicology and Chemistry (SETAC) Other Titles from the Society of Environmental Toxicology and Chemistry (SETAC) Ecological Assessment of Selenium in the Aquatic Environment Linking Aquatic CEhxpaopsmuaren ,a Andda Emffse, cBtsr:o Rokissk, eAdsisteosrssm ent of Pesticides Brock, Alix, Brown, Capri, Gottesbüren2, 0H1e0imbach, Lythgo, Schulz, Streloke, editors 2009 Application of Uncertainty Analysis to Ecological Risk of Pesticides Derivation and Use of EnvironWmaernrteanl -QHuicaklist,y H aanrdt ,H eudmitoarns Health Standards for Chemical Substances 2in0 1W0ater and Soil Crane, Matthiessen, Maycock, Merrington, Whitehouse, editors Linking Aquatic Exposure and Ef2f0e0ct9s: Risk Assessment of Pesticides Brock, Alix, Brown, Capri, Gottesbüren, Heimbach, Lythgo, Schulz, Streloke, editors Aquatic Macrophyte Ri2s0k1 A0ssessment for Pesticides Maltby, Arnold, Arts, Davies, Heimbach, Pickl, Poulsen, editors Ecological Models for Regulatory Risk Assessmen2t0s0 o9f Pesticides: Developing a Strategy for the Future Thorbek, Forbes, Heimbach, Hommen, Thulke, Van den Brink, Wogram, Grimm, editors Veterinary Medici2n0e1s0 in the Environment Crane, Boxall, Barrett 2008 Derivation and Use of Environmental Quality and Human Health Standards for Chemical Substances in Water and Soil Relevance of Ambient Water Quality Criteria for Ephemeral and Effluent-dependent Crane, Matthiessen, Maycock, Merrington, Whitehouse, editors Watercourses of the Arid Western United States 2010 Gensemer, Meyerhof, Ramage, Curley 2008 Aquatic Macrophyte Risk Assessment for Pesticides Maltby, Arnold, Arts, Davies, Heimbach, Pickl, Poulsen Extrapolation Practice for Ecotoxicological Effect Characterization of Chemicals 2010 Solomon, Brock, de Zwart, Dyev, Posthumm, Richards, editors 2008 Veterinary Medicines in the Environment Crane, Boxall, Barrett Environmental Life Cycle Costing 2008 Hunkeler, Lichtenvort, Rebitzer, editors 2008 Relevance of Ambient Water Quality Criteria for Ephemeral and Effluent dependent Watercourses of the Arid Western United States Valuation of Ecological Resources: Integration of Ecology and Socioeconomics Gensemer, Meyerhof, Ramage, Curley in Environmental Decision Making 2008 Stahl, Kapustka, Munns, Bruins, editors 2007 For information about SETAC publications, including SETAC’s international journals, Environmental Toxicology and Chemistry and Integrated Environmental Assessment and Management, contact the SETAC office nearest you: SETAC SETAC Office 1010 North 12th Avenue Avenue de la Toison d’Or 67 Pensacola, FL 32501-3367 USA B-1060 Brussells, Belguim T 850 469 1500 F 850 469 9778 T 32 2 772 72 81 F 32 2 770 53 86 E [email protected] E [email protected] www.setac.org Environmental Quality Through Science® 64169.indb 2 5/3/10 10:19:46 AM Ecotoxicology of Amphibians and Reptiles Second Edition Edited by Donald W. 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Trademark Notice: Product or corporate names may be trademarks or registered trademarks, and are used only for identification and explanation without intent to infringe. Library of Congress Cataloging-in-Publication Data Ecotoxicology of amphibians and reptiles / editors, Donald W. Sparling … [et al.]. -- 2nd ed. p. cm. Includes bibliographical references and index. ISBN 978-1-4200-6416-2 (hardcover : alk. paper) 1. Amphibians--Effect of pollution on. 2. Reptiles--Effect of pollution on. I. Sparling, D. W. (Donald W.) II. Title. 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The publications provide information for keeping abreast of recent developments in familiar subject areas and for rapid introduction to principles and approaches in new subject areas. SETAC recognizes and thanks the past coordinating editors of SETAC books: A.S. Green, International Zinc Association Durham, North Carolina, USA C.G. Ingersoll, Columbia Environmental Research Center US Geological Survey, Columbia, Missouri, USA T.W. La Point, Institute of Applied Sciences University of North Texas, Denton, Texas, USA B.T. Walton, US Environmental Protection Agency Research Triangle Park, North Carolina, USA C.H. Ward, Department of Environmental Sciences and Engineering Rice University, Houston, Texas, USA 64169.indb 5 5/3/10 10:19:47 AM Cover photo credits Sampling in the Sierras: With permission from Deborah F. Cowman, Executive Director, Brazos Valley Museum of Natural History, Bryan, Texas. Western fence lizard: With permission from Bill Bouton, http://www.flickr.com/photos/billbouton /sets Pacific tree frog skeletal view: With permission from Brandon Ballengée, “The Complex Life- Cycle of the Trematode, Riberoria ondatrae” by Brandon Ballengée, 2002, 11 by 14 inches. Sakura Ink on water-colour paper. Courtesy the artist and Archibald Arts, New York, NY. Collection of Anthony Archibald J. Figure is from Rohr, J.R., T. Raffel, and S.K. Sessions. (2008). Parasites and Amphibians. Chapter 4. In: Amphibian Biology, Conservation and Decline of Amphibians (H, Heatwole, ed.) Chipping Norton, Australia: Surrey Beatty & Sons. Pacific tree frog: By Gary Fellers, US Geological Survey, copyright free. European pond turtle: With permission from Manuel Ortiz Santaliestra, Instituto de Investigación en Recursos Cinegéticos, Ciudad Real, Spain. 64169.indb 6 5/3/10 10:19:47 AM Contents List of Figures ...................................................................................................................................ix List of Tables ..................................................................................................................................xiii About the Editors ...........................................................................................................................xvii List of Contributors .........................................................................................................................xix Acknowledgments ...........................................................................................................................xxi Preface for Second Edition ..........................................................................................................xxiii Preface from the First Edition........................................................................................................xxv Chapter 1 Recent Advancements in Amphibian and Reptile Ecotoxicology ...............................1 Donald W. Sparling, Greg Linder, Christine A. Bishop, and Sherry K. Krest Chapter 2 Declines and the Global Status of Amphibians .........................................................13 Ross A. Alford Chapter 3 The Global Status of Reptiles and Causes of Their Decline ......................................47 Brian D. Todd, John D. Willson, and J. Whitfield Gibbons Chapter 4 Ecotoxicology of Amphibians and Reptiles in a Nutshell .........................................69 Greg Linder, Christine M. Lehman and Joseph R. Bidwell Chapter 5 Physiological Ecology of Amphibians and Reptiles: Natural History and Life History Attributes Framing Chemical Exposure in the Field....................105 Greg Linder, Brent D. Palmer, Edward E. Little, Christopher L. Rowe, and Paula F.P. Henry Chapter 6 Effects of Current-Use Pesticides on Amphibians ...................................................167 Christine M. Lehman and Bethany K. Williams Chapter 7 Ecotoxicology of Pesticides in Reptiles ...................................................................203 Bruce D. Pauli, Stacey Money, and Donald W. Sparling Chapter 8 Atrazine in the Environment and Its Implications for Amphibians and Reptiles ....225 Christine A. Bishop, Tana V. McDaniel, and Shane R. de Solla Chapter 9 Ecotoxicology of Organic Contaminants to Amphibians ........................................261 Donald W. Sparling vii 64169.indb 7 5/3/10 10:19:47 AM viii Contents Chapter 10 Organic Contaminants in Reptiles ...........................................................................289 Shane R. de Solla Chapter 11 Interdisciplinary and Hierarchical Approaches for Studying the Effects of Metals and Metalloids on Amphibians ................................................................325 W.A. Hopkins and Christopher. L. Rowe Chapter 12 The Ecotoxicology of Metals in Reptiles .................................................................337 Britta Grillitsch and Luis Schiesari Chapter 13 Solar UV Radiation and Amphibians: Factors Mitigating Injury ............................449 Edward E. Little and Robin D. Calfee Chapter 14 Multiple Stressors and Indirect Food Web Effects of Contaminants on Herptofauna .........................................................................................................475 Rick A. Relyea Chapter 15 Emerging Contaminants and Their Potential Effects on Amphibians and Reptiles ..............................................................................................................487 Laura L. McConnell and Donald W. Sparling Chapter 16 A Decade of Deformities: Advances in Our Understanding of Amphibian Malformations and Their Implications .............................................511 Pieter T.J. Johnson, Mari K. Reeves, Sherry K. Krest, and Alfred E. Pinkney Chapter 17 Population Estimation Methods for Amphibians and Reptiles ................................537 Larissa L. Bailey and Marc J. Mazerolle Chapter 18 Epilogue: Ecotoxicology of Amphibians and Reptiles — Where Should We Be Going and How Do We Get There? ..............................................................547 Greg Linder, Christine A. Bishop, Sherry K. Krest, and Donald W. Sparling Appendix: Metal Contamination in Reptiles: An Appendix of Data Compiled from the Existing Literature ......................................................................................................553 Britta Grillitsch and Luis Schiesari Index ..............................................................................................................................................905 64169.indb 8 5/3/10 10:19:48 AM List of Figures Figure 1.1 Total number of contaminant-related papers published between 1996 and 2008 by vertebrate class. ................................................................................3 Figure 1.2 Annual numbers of scientific publications for amphibians and reptiles between 1996 and 2008 as listed in ISI Web of Science. ......................................4 Figure 1.3 Number of contaminant-related papers published for amphibians and reptiles between 1996 and 2008 ............................................................................5 Figure 1.4 Percent of all scientific publications for amphibians and reptiles between 1996 and 2008 that were contaminant related. .................................................5 Figure 1.5 Contaminant-related papers published on amphibians between 1996 and 2008 by chemical class ..................................................................................6 Figure 1.6 Contaminant-related papers for amphibians that were published between 1996 and 2008 by taxonomic group ......................................................................6 Figure 1.7 A comparison of the numbers of papers published for amphibians between 1996 and 2008 by associated stressor. ...................................................................7 Figure 1.8 Number of contaminant-related papers published between 1996 and 2008 on reptiles by type of contaminant. .......................................................................7 Figure 1.9 Number of reptile contaminant-related papers published between 1996 and 2008 by taxonomic group. .....................................................................................8 Figure 1.10 A comparison of the number of contaminant- and disease-related papers published annually for reptiles from 1996 to 2008 ...............................................8 Figure 2.1 Percentage of amphibian species with extant populations in nature in each IUCN threat category for which 6 categories of threats are believed to be operating .............................................................................................................17 Figure 3.1 Status of the major lineages of reptiles according to the World Conservation Union (IUCN) Red List in 2009 ...................................................57 Figure 5.1 The conceptual model of energy and material flow provides a physiological energetics framework for evaluating exposure with traditional food chain models ............................................................................108 Figure 10.1 Cladistic classification of “reptiles” based upon monophyletic groupings .......290 Figure 10.2 Biphenyl and polychlorinated biphenyls; both non-ortho (PCB 126) and ortho (PCBs 153 and 187) chlorinated biphenyls are described .......................298 Figure 10.3 Polychlorinated dibenzo-p-dioxins and furans; the most toxic forms (2,3,7,8-chlorine-substituted) congeners are displayed .....................................300 Figure 10.4 Examples of the relative proportion of body burdens of organochlorine pesticides (DDE, chlordane), PCBs, and PBDEs in a variety of animals, including watersnakes, turtles, and alligators ...................................................300 ix 64169.indb 9 5/3/10 10:19:48 AM x List of Figures Figure 10.5 Two organochlorine pesticides, p,p’-DDE and chlordane, which are among the most common OC pesticides detected in biota ...........................................303 Figure 10.6 Three examples of polycyclic aromatic hydrocarbons often found in the environment .......................................................................................................308 Figure 10.7 The surfactants perfluorooctane sulfonate and perfluorooctanoic acid ............309 Figure 10.8 Polybrominated diphenyl ethers; BDE 99 is typically found in penta formulations, whereas BDE 209 is found in the deca formulation ...................310 Figure 10.9 Hydrocarbons found in crude oil mixtures and in some petroleum products; asphaltene is highly variable .............................................................312 Figure 10.10 Oral LD50s of selected organic contaminants to rats; the lower the value, the greater the toxicity .......................................................................................314 Figure 12.1 Periodic table of elements showing the metallic elements included in the present review, and their classification according to their biological and ecotoxicological relevance. ................................................................................339 Figure 12.2 Chronology of the cumulative number of publications dealing with the ecotoxicology of metals in reptiles. ...................................................................341 Figure 12.3 Distribution of 109Cd among reproductive tissues in female painted turtles, Chrysemys picta, 6, 24, and 192 hours after intravascular injection ................387 Figure 12.4 Distribution of mercury, cadmium, manganese, copper, iron, and zinc among oviductal egg compartments in loggerhead turtles, Caretta caretta .....388 Figure 12.5 Distribution of cadmium, copper, and mercury among reproductive and nonreproductive tissues of female loggerhead turtle, Caretta caretta ..............390 Figure 12.6 Distribution of cadmium among tissues of American alligators, Alligator mississippiensis, 10 days after cadmium administration (single intracardiac injection of CdCl , 1.0 mg/kg body mass) ...................................394 2 Figure 12.7 Mean mercury concentrations in tissues of wild and farm-raised American alligators, Alligator mississippiensis .................................................................394 Figure 12.8 Mean lead concentrations in tissues of Chelydra serpentina in the Old Lead Belt region (Missouri) ..............................................................................396 Figure 12.9 Distribution of information on metal concentrations in reptiles as indicated by the numbers of publications per reptile order and suborder, and metal. ......403 Figure 13.1 Sunburn and lesions on a juvenile Ambystoma tigrinum exposed to low-level irradiance in the laboratory. ...............................................................451 Figure 13.2 Absorbance scans for tannic acid, tea, and water from oak leaves soaked for 2 months. ......................................................................................................455 Figure 13.3 Decreases in dissolved organic carbon increases UV-B exposure in the water column in sites in Minnesota. ..................................................................455 Figure 13.4 (A) Average oviposition depth for Ambystoma gracile egg masses at 3 sites within Mt. Rainier National Park, Washington. (B) Dissolved organic carbon concentration of water from 3 sites within Mt. Rainier National Park, Washington ..............................................................................................459 64169.indb 10 5/3/10 10:19:48 AM